Attack of the Rock-Eating Microbes!Some bacteria break down minerals, while others make them

Sid Perkins

Geologists are studying bacteria nowadays. It's not that the rock hounds have gone soft. Instead, they've found that geological processes once attributed solely to simple inorganic chemistry have microbial fingerprints all over them. In rocky venues ranging from abandoned mines in California to water wells in Bangladesh to hydrothermal vents on the seafloor, bacteria are at work. If the
microbes aren't driving the underlying chemical reactions in those places, they're at least taking advantage of the energy that's being released by these reactions.

Researchers are finding that bacteria living on the seafloor may be key players in the chemical reactions that slowly transform the rocks there, and in the process, help balance ocean chemistry. Others are discovering that microbes can create tiny mineral particles by extracting exceedingly small concentrations of dissolved metals from the fluids that course through soils and sediments. In at least one instance, bacteria probably created a significant deposit of high-value mineral ore (see "Microbial Machinations," below).

Heavy metal

Geochemists are finding that mineral-eating bacteria can be partly to blame for major environmental problems. For instance, when mines go bust, they often leave behind a mix of water and minerals that bacteria can convert into acidic runoff that's deadly to plants and animals.

ACID STREAM. Bacteria accelerate the formation of acidic mine drainage, an environmental problem that taints more than 19,000 kilometers of streams and rivers nationwide.

Pennsylvania Department of Environmental Protection

Nationwide, acidic mine drainage affects more than 19,000 kilometers of rivers and streams. Some scientists rate toxic mine drainage as the greatest water-quality problem facing the western United States. In Colorado alone, the effluent from more than 7,000 abandoned mines contaminates more than 2,500 km of streams, says Diane McKnight, a geologist at the University of Colorado in Boulder.

Consider the Richmond Mine in California's Iron Mountain, about 15 kilometers northwest of Redding. Active from the late 1800s until the 1960s, the mine yielded a bounty of iron, silver, gold, zinc, and copper ores. All of the blasting and tunneling that went on at the site riddled the mountain with fractures, exposing enormous areas of rock and mineral deposits to oxygen and water.

When that combination includes sulfide minerals, the sulfuric acid that's produced leaches toxic metals out of the rock, says Jill Banfield, a geochemist at the University of California, Berkeley. But it's the presence of particular microbes that really aggravate the situation.

For instance, the oxidation of iron exposed by mining typically takes place more slowly in acidic conditions than in solutions with neutral pH. However, acid-tolerant microorganisms can accelerate the oxidation reaction and harness the energy it provides. This process also speeds up the mineral breakdown and releases up to 10 times as many metal ions into the water as sterile acid runoff would.

Waters draining through Iron Mountain and collecting in the mining tunnels have a pH between 0 and 1, about the same as that of battery acid. According to the Environmental Protection Agency, Iron Mountain at one time yielded the most acidic mine drainage in the world. Chemical analyses by Banfield and her colleagues show that dissolved in each liter of today's drainage can be up to 80 grams, or a heaping teaspoon, of dissolved iron and as much as 6 g of zinc. Other trace elements include copper and arsenic.

Before cleanup efforts began there in the late 1980s, acidic runoff from Iron Mountain annually dumped into local streams about a ton of dissolved copper and zinc—about one-quarter of the total national discharge of those metals from industrial and other point sources each year.

Most efforts to clean up bacterially exacerbated acidic mine drainage focus on treating the effluent after it's created. However, processes that reduce the concentration of dissolved oxygen and thus limit bacterial growth in mine fluids might prevent much of the acid production in the first place, says McKnight.

Unwell wells

In some parts of the world, mineral-munching bacteria may be releasing heavy metals directly into people's drinking water. Arsenic exposure from well water tainted in this way is particularly widespread in Bangladesh, where millions of people rely on well water that courses through arsenic-containing rock (SN: 11/23/02, p. 325). Chronic exposure to even small amounts of arsenic in drinking water increases a person's risk of cancer and other diseases, and the element disrupts some of the body's hormonal systems (SN: 3/17/01, p. 164).

The most prevalent arsenic-bearing compounds in minerals are arsenates. These compounds strongly bind to several common minerals, so they don't typically dissolve into waters flowing through underground reservoirs, says Ronald S. Oremland of the U.S. Geological Survey in Menlo Park, Calif. Problems arise when chemical reactions change the arsenates into arsenites, which don't bind tightly to other minerals and can therefore enter the underground water supply.

Evidence is now mounting that organic matter and the microbes it feeds may be playing a role in the formation of arsenites in aquifers. Scientists have isolated and identified 16 different microbes that can feed on arsenic, says Oremland. They're found in many different environments including hot springs, gold mines, highly alkaline lakes, and the gastrointestinal tracts of people and other animals. Some extract the energy from oxidation reactions, in which the arsenic atoms end up losing electrons, and others tap into reduction reactions, in which the arsenic atoms gain electrons. "These microbes make a living off what's normally considered to be a potent toxin," he notes.

The organisms, which come from at least nine different groups of microbes, can engage arsenic in a variety of chemical reactions. Oremland and John F. Stolz, a microbiologist at Duquesne University in Pittsburgh, discussed what they call "the ecology of arsenic" in the May 9 Science.

The arsenic-metabolizing organisms don't dine exclusively on compounds bearing that one element, says Oremland. Several can also gain energy from reactions involving sulfate compounds. One species, Sulfurospirillum barnesii, can metabolize no fewer than nine types of atoms or ions other than arsenates, including sulfur, nitrates, nitrites, and selenates.

Part of the solution to this arsenic problem may be to nurture soil microbes that would lock down arsenic compounds instead of releasing them. In Bangladesh, geologists experimented with this approach by injecting into a tainted aquifer large amounts of nitrates that would theoretically nourish some desirable bacteria. The test produced a rapid and dramatic decrease in the concentration of arsenic in the water from nearby wells. The result suggests the presence of a thriving community of anaerobic microbes that used the nitrates as fuel and converted the poisonous arsenites in the water to less-soluble arsenates.

Also supporting that scenario, says Oremland, other scientists have cultured arsenic-metabolizing microbes from sediments drilled from tainted aquifers in Bangladesh.

Soggy crust

Just as arsenic in aquifers and sulfide minerals in mines can nurture pollution-enhancing bacteria, lava-derived minerals in the seafloor may be nourishing mineral-metabolizing microbes. Some scientists suspect that the deep-sea phenomenon may be vast enough to transform the chemical composition of the ocean floor. Because more than 70 percent of Earth's surface is ocean bottom, these mineral beds could actually amount to one of the planet's largest ecosystems.

FILM STARS. Bacteria in the low-oxygen fluids of an abandoned mine created these zinc sulfide spheres. Like most other mineral particles assembled by microbes, these have a consistent size, shape, and chemical composition.

Banfield

Chemical analyses of basalt drilled from the ocean floor show that in new rock being extruded from midocean ridges, only about 15 percent of the iron atoms are ions that have a triple dose of positive charge. Core samples of older seafloor rocks indicate that after 10 million to 20 million years of exposure to seawater, that form of ion—the same type generated by bacteria in acidic mine runoff—makes up around 45 percent of the iron atoms. Over the same period, approximately 70 percent of the sulfides originally present in the basalt have dissolved.

While some scientists have held that microbes play a significant role in these lethargic mineral transformations, no one could identify the metabolic mechanisms that any such organisms might use, says Katrina J. Edwards, a geochemist at Woods Hole (Mass.) Oceanographic Institution. A series of experiments by Edwards and her colleagues suggests that iron-oxidizing bacteria may indeed play a part in the so-called weathering of ocean-floor minerals.

First, the researchers used deep-diving robots to obtain samples of sulfide minerals from a seafloor hydrothermal vent off the coast of Washington State. To create surfaces that would reveal seafloor-bacterial effects, the scientists polished and sterilized the minerals before returning them in July 2000 to the ocean floor near the vent site. Other sterilized samples, including pure sulfur and other sulfur-bearing minerals collected around the world, were placed in the same test location. The frigid waters surrounding the samples, about 2,400 meters below the ocean's surface, held few dissolved metals and no detectable hydrogen sulfide.

When the researchers retrieved the samples less than 2 months later, each of the iron-bearing sulfide samples had a pitted, microbe-infested surface that was coated with iron oxide particles. The thickest accumulation, up to 1 millimeter in spots, appeared on the sulfide fragment originally taken from the seafloor vent, says Edwards. She and her colleagues reported these findings in the Aug. 1 Geochimica et Cosmochimica Acta.

In follow-up laboratory experiments, Edwards and other scientists examined those weathered vent minerals and cultured microbes that had colonized the sterilized samples' surfaces. Analyses of the organisms' DNA distinguished nine species of bacteria, all of which starved in the lab if they weren't provided with iron-bearing minerals or solutions containing dissolved iron. Even sugar solutions, on which bacteria normally thrive, didn't supply the proper nutrients, says Edwards. The microbes grew best in water temperatures ranging from 3°C to 10°C and on the surface of sulfide rocks that the researchers had retrieved from the hydrothermal vent.

The evidence that microbes are transforming vast volumes of ocean crust remains circumstantial, says Edwards. However, she and other scientists now have an idea of where to look for direct evidence.

If iron-oxidizing microbes do thrive within the 500 m of seafloor basalt through which ocean water slowly circulates, Edwards notes, "it's a huge environment." That volume of rock far exceeds that of the more biologically productive sunlit zone of the ocean, which extends down from the sea's surface only about 100m.

Microbes leave footprints. When they assemble minerals, they create particles with distinctive sizes and shapes. Such patterns can help scientists, including geochemist Katrina J. Edwards of Woods Hole (Mass.) Oceanographic Institution, identify where bacteria are having geochemical and mineralogical effects.

In Edwards' lab, cultures of iron-oxidizing bacteria produced iron oxide particles that appeared to grow at the surface of the cells or within a capsulelike layer around them. Particles measured between 2 nanometers and 2 micrometers across, and most aggregates of particles were less than 5 µm in diameter.

Other scientists have caught bacteria in the act of making minerals, too. In 2000, Jill Banfield, a geochemist at the University of California, Berkeley, and her colleagues reported formation of zinc sulfide particles by bacteria living in a flooded tunnel of an abandoned lead mine near Tennyson, Wis. In the low-oxygen conditions there, thick mats of sulfate-reducing bacteria grew on the carbonate rocks. As the microbes extracted energy from sulfates dissolved in the mine waters, they produced sulfide ions that chemically bonded to dissolved zinc. Individual particles of zinc sulfide were about 3 nm across and aggregated into spherical clumps about 3 µm in diameter.

The concentration of zinc in the bacterial mats was about 1 million times that of dissolved zinc in the surrounding water, says Banfield. Also, the mineral particles contained no lead and only trace amounts of impurities such as iron or arsenic.

Such purity is a sure sign that microbes assembled the mineral particles, says Thomas M. Bawden of the company Global Mineral Resources in San Francisco. Deposits of zinc sulfide ore that weren't created by bacteria often contain as much as 10 percent iron, as well as significant quantities of arsenic and lead.

In the October Geology, Bawden and his colleagues publish their analyses of samples from a massive zinc sulfide deposit located in a gold mine in Nevada. Several characteristics of the minerals taken from the deepest portion of that deposit suggest that the sulfide formations there were assembled by microbes.

First, the particles are spherical and measure less than 1 µm in diameter. Also, they're pure zinc sulfide. Finally, the particles contain a much smaller fraction of sulfur-34 isotopes than normal—a characteristic that Bawden says is a "smoking gun" for biological activity. That's because bacteria usually react more readily with compounds that contain lighter isotopes of sulfur. In all, the Nevada deposit contains about 400,000 metric tons of seemingly bacteria-produced sulfides.

The sediments containing the ore are capped by a layer of volcanic ash that was laid down about 15.5 million years ago, so the Nevada sulfide deposits probably were produced between 16 million and 20 million years ago, says Bawden. If the volcanic ash hadn't entombed the sulfide deposits, all evidence of the bacteria-produced minerals might have disappeared. At the time of the ancient eruption that produced the ash, Nevada's climate was arid and the water table was dropping, conditions that would have exposed the upper layers of the deposit to sulfide-destroying oxygen.

There's no reason to think that similar mineral deposits aren't being created by microbes in many places on Earth today, says Bawden.